Membrane curvature in cell biology: An integration of molecular mechanisms

Journal of Cell Biology

Volumn 214, Issue 4, 2016, Pages 375-387

  Jarsch, Iris K ^a   Daste, Frederic ^a   Gallop, Jennifer L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; CELL MEMBRANE; CELL NUCLEUS; CELL SHAPE; CHLOROPLAST; CYTOLOGY; ENDOSOME; LIPID BILAYER; MITOCHONDRION; NONHUMAN; OLIGOMERIZATION; PLANT CELL; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; HUMAN; METABOLISM; SECRETORY PATHWAY;

ANIMALS; BIOMECHANICAL PHENOMENA; CELL MEMBRANE; CELL SHAPE; ENDOSOMES; HUMANS; MODELS, BIOLOGICAL; SECRETORY PATHWAY;

EID: 84983343696     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201604003     Document Type: Review

References (126)

1. Alkhaja, A.K., D.C. Jans, M. Nikolov, M. Vukotic, O. Lytovchenko, F. Ludewig, W. Schliebs, D. Riedel, H. Urlaub, S. Jakobs, and M. Deckers. 2012. MIN OS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization. Mol. Biol. Cell. 23:247-257. http ://dx.doi.org /10.1091 /mbc.E11 -09 -0774
2. Anderson, D.J., and M.W. Hetzer. 2008. Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. J. Cell Biol. 182:911-924. http ://dx.doi.org /10.1083 /jcb.200805140
3. Antonny, B., J. Bigay, J.F. Casella, G. Drin, B. Mesmin, and P. Gounon. 2005. Membrane curvature and the control of GTP hydrolysis in Arf1 during COPI vesicle formation. Biochem. Soc. Trans. 33:619-622. http ://dx.doi .org /10.1042 /BST0330619
4. Armbruster, U., M. Labs, M. Pribil, S. Viola, W. Xu, M. Scharfenberg, A.P. Hertle, U. Rojahn, P.E. Jensen, F. Rappaport, et al. 2013. Arabidopsis CUR VAT URE THY LAK OID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell. 25:2661-2678. http ://dx.doi .org /10.1105 /tpc.113.113118
5. Audhya, A., A. Desai, and K. Oegema. 2007. A role for Rab5 in structuring the endoplasmic reticulum. J. Cell Biol. 178:43-56. http ://dx.doi.org /10 .1083 /jcb.200701139
6. Avinoam, O., M. Schorb, C.J. Beese, J.A. Briggs, and M. Kaksonen. 2015. Endocytic sites mature by continuous bending and remodeling of the clathrin coat. Science. 348:1369-1372. http ://dx.doi.org /10.1126 /science .aaa9555
7. Bagatolli, L.A., and O.G. Mouritsen. 2013. Is the fluid mosaic (and the accompanying raft hypothesis) a suitable model to describe fundamental features of biological membranes? What may be missing? Front. Plant Sci. 4:457. http ://dx.doi.org /10.3389 /fpls.2013.00457
8. Barbot, M., D.C. Jans, C. Schulz, N. Denkert, B. Kroppen, M. Hoppert, S. Jakobs, and M. Meinecke. 2015. Mic10 oligomerizes to bend mitochondrial inner membranes at cristae junctions. Cell Metab. 21:756-763. http ://dx.doi .org /10.1016 /j.cmet.2015.04.006
9. Barelli, H., and B. Antonny. 2009. Cell biology: Detached membrane bending. Nature. 458:159-160. http ://dx.doi.org /10.1038 /458159a
10. Baumann, O., and B. Walz. 2001. Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int. Rev. Cytol. 205:149-214. http ://dx.doi.org /10.1016 /S0074 -7696(01)05004 -5
11. Bayer, E.M., S. Mongrand, and J. Tilsner. 2014. Specialized membrane domains of plasmodesmata, plant intercellular nanopores. Front. Plant Sci. 5:507. http ://dx.doi.org /10.3389 /fpls.2014.00507
12. Beck, R., Z. Sun, F. Adolf, C. Rutz, J. Bassler, K. Wild, I. Sinning, E. Hurt, B. Brügger, J. Béthune, and F. Wieland. 2008. Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc. Natl. Acad. Sci. USA. 105:11731-11736. http ://dx.doi.org /10.1073 /pnas.0805182105
13. Bezanilla, M., A.S. Gladfelter, D.R. Kovar, and W.L. Lee. 2015. Cytoskeletal dynamics: a view from the membrane. J. Cell Biol. 209:329-337. http ://dx.doi.org /10.1083 /jcb.201502062
14. Bi, X., R.A. Corpina, and J. Goldberg. 2002. Structure of the Sec23/24-Sar1 pre-budding complex of the COP II vesicle coat. Nature. 419:271-277. http ://dx.doi.org /10.1038 /nature01040
15. Bigay, J., P. Gounon, S. Robineau, and B. Antonny. 2003. Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature. Nature. 426:563-566. http ://dx.doi.org /10.1038 /nature02108
16. Boucrot, E., A.P. Ferreira, L. Almeida-Souza, S. Debard, Y. Vallis, G. Howard, L. Bertot, N. Sauvonnet, and H.T. McMahon. 2015. Endophilin marks and controls a clathrin-independent endocytic pathway. Nature. 517:460-465. http ://dx.doi.org /10.1038 /nature14067
17. Boulant, S., C. Kural, J.C. Zeeh, F. Ubelmann, and T. Kirchhausen. 2011. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 13:1124-1131. http ://dx.doi.org /10.1038 / ncb2307
18. Bridges, A.A., M.S. Jentzsch, P.W. Oakes, P. Occhipinti, and A.S. Gladfelter. 2016. Micron-scale plasma membrane curvature is recognized by the septin cytoskeleton. J. Cell Biol. 213:23-32. http ://dx.doi.org /10.1083 / jcb.201512029
19. Busch, D.J., J.R. Houser, C.C. Hayden, M.B. Sherman, E.M. Lafer, and J.C. Stachowiak. 2015. Intrinsically disordered proteins drive membrane curvature. Nat. Commun. 6:7875. http ://dx.doi.org /10.1038 /ncomms8875
20. Caltagarone, J., S. Ma, and A. Sorkin. 2015. Dopamine transporter is enriched in filopodia and induces filopodia formation. Mol. Cell. Neurosci. 68:120-130. http ://dx.doi.org /10.1016 /j.mcn.2015.04.005
21. Carlton, J., M. Bujny, B.J. Peter, V.M. Oorschot, A. Rutherford, H. Mellor, J. Klumperman, H.T. McMahon, and P.J. Cullen. 2004. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr. Biol. 14:1791-1800. http ://dx.doi.org /10.1016 /j.cub.2004.09.077
22. Cashikar, A.G., S. Shim, R. Roth, M.R. Maldazys, J.E. Heuser, and P.I. Hanson. 2014. Structure of cellular ESC RT-III spirals and their relationship to HIV budding. eLife. http ://dx.doi.org /10.7554 /eLife.02184
23. Chang-Ileto, B., S.G. Frere, R.B. Chan, S.V. Voronov, A. Roux, and G. Di Paolo. 2011. Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev. Cell. 20:206-218. http ://dx.doi.org /10.1016 /j.devcel.2010.12.008
24. Chappie, J.S., J.A. Mears, S. Fang, M. Leonard, S.L. Schmid, R.A. Milligan, J.E. Hinshaw, and F. Dyda. 2011. A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell. 147:209-222. http ://dx.doi.org /10.1016 /j.cell.2011.09.003
25. Chen, Z., Z. Shi, and T. Baumgart. 2015. Regulation of membrane-shape transitions induced by I-BAR domains. Biophys. J. 109:298-307. http ://dx.doi.org /10.1016 /j.bpj.2015.06.010
26. Cheng, J.P., C. Mendoza-Topaz, G. Howard, J. Chadwick, E. Shvets, A.S. Cowburn, B.J. Dunmore, A. Crosby, N.W. Morrell, and B.J. Nichols. 2015. Caveolae protect endothelial cells from membrane rupture during increased cardiac output. J. Cell Biol. 211:53-61. http ://dx.doi.org /10 .1083 /jcb.201504042
27. Chiaruttini, N., L. Redondo-Morata, A. Colom, F. Humbert, M. Lenz, S. Scheuring, and A. Roux. 2015. Relaxation of loaded ESC RT-III spiral springs drives membrane deformation. Cell. 163:866-879. http ://dx.doi .org /10.1016 /j.cell.2015.10.017
28. Collins, A., A. Warrington, K.A. Taylor, and T. Svitkina. 2011. Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr. Biol. 21:1167-1175. http ://dx.doi.org /10.1016 /j.cub .2011.05.048
29. Copic, A., C.F. Latham, M.A. Horlbeck, J.G. D'Arcangelo, and E.A. Miller. 2012. ER cargo properties specify a requirement for COP II coat rigidity mediated by Sec13p. Science. 335:1359-1362. http ://dx.doi.org /10.1126 /science.1215909
30. Dagdas, Y.F., K. Yoshino, G. Dagdas, L.S. Ryder, E. Bielska, G. Steinberg, and N.J. Talbot. 2012. Septin-mediated plant cell invasion by the rice blast fungus, Magnaporthe oryzae. Science. 336:1590-1595. http ://dx.doi.org /10.1126 /science.1222934
31. Daumke, O., R. Lundmark, Y. Vallis, S. Martens, P.J. Butler, and H.T. McMahon. 2007. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature. 449:923-927. http ://dx.doi .org /10.1038 /nature06173
32. Day, C.A., N.W. Baetz, C.A. Copeland, L.J. Kraft, B. Han, A. Tiwari, K.R. Drake, H. De Luca, D.J. Chinnapen, M.W. Davidson, et al. 2015. Microtubule motors power plasma membrane tubulation in clathrin-independent endocytosis. Traffic. 16:572-590. http ://dx.doi.org /10.1111 /tra.12269
33. Delevoye, C., S. Miserey-Lenkei, G. Montagnac, F. Gilles-Marsens, P. Paul- Gilloteaux, F. Giordano, F. Waharte, M.S. Marks, B. Goud, and G. Raposo. 2014. Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Reports. 6:445-454. http ://dx.doi.org /10.1016 /j.celrep.2014.01.002
34. Ding, B., J.S. Haudenshield, R.J. Hull, S. Wolf, R.N. Beachy, and W.J. Lucas. 1992. Secondary plasmodesmata are specific sites of localization of the tobacco mosaic virus movement protein in transgenic tobacco plants. Plant Cell. 4:915-928. http ://dx.doi.org /10.1105 /tpc.4.8.915
35. Doucet, C.M., and M.W. Hetzer. 2010. Nuclear pore biogenesis into an intact nuclear envelope. Chromosoma. 119:469-477. http ://dx.doi.org /10.1007 /s00412 -010 -0289 -2
36. Estrada, P., J. Kim, J. Coleman, L. Walker, B. Dunn, P. Takizawa, P. Novick, and S. Ferro-Novick. 2003. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163:1255-1266. http ://dx.doi.org /10.1083 /jcb.200304030
37. Fernandez-Calvino, L., C. Faulkner, J. Walshaw, G. Saalbach, E. Bayer, Y. Benitez-Alfonso, and A. Maule. 2011. Arabidopsis plasmodesmal proteome. PLoS One. 6:e18880. http ://dx.doi.org /10.1371 /journal.pone .0018880
38. Ford, M.G., I.G. Mills, B.J. Peter, Y. Vallis, G.J. Praefcke, P.R. Evans, and H.T. McMahon. 2002. Curvature of clathrin-coated pits driven by epsin. Nature. 419:361-366. http ://dx.doi.org /10.1038 /nature01020
39. Fotin, A., Y. Cheng, P. Sliz, N. Grigorieff, S.C. Harrison, T. Kirchhausen, and T. Walz. 2004. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature. 432:573-579. http ://dx.doi.org /10 .1038 /nature03079
40. Frick, M., N.A. Bright, K. Riento, A. Bray, C. Merrified, and B.J. Nichols. 2007. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr. Biol. 17:1151-1156. http ://dx.doi.org /10.1016 /j.cub.2007.05.078
41. Frost, A., R. Perera, A. Roux, K. Spasov, O. Destaing, E.H. Egelman, P. De Camilli, and V.M. Unger. 2008. Structural basis of membrane invagination by F-BAR domains. Cell. 132:807-817. http ://dx.doi.org /10.1016 /j.cell .2007.12.041
42. Gallop, J.L., C.C. Jao, H.M. Kent, P.J. Butler, P.R. Evans, R. Langen, and H.T. McMahon. 2006. Mechanism of endophilin N-BAR domainmediated membrane curvature. EMBO J. 25:2898-2910. http ://dx.doi.org /10.1038 /sj.emboj.7601174
43. Grabski, S., A.W. De Feijter, and M. Schindler. 1993. Endoplasmic reticulum forms a dynamic continuum for lipid diffusion between contiguous soybean root cells. Plant Cell. 5:25-38. http ://dx.doi.org /10.1105 /tpc.5.1.25
44. Grison, M.S., L. Brocard, L. Fouillen, W. Nicolas, V. Wewer, P. Dörmann, H. Nacir, Y. Benitez-Alfonso, S. Claverol, V. Germain, et al. 2015. Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell. 27:1228-1250. http ://dx.doi.org /10 .1105 /tpc.114.135731
45. Guerrier, S., J. Coutinho-Budd, T. Sassa, A. Gresset, N.V. Jordan, K. Chen, W.L. Jin, A. Frost, and F. Polleux. 2009. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell. 138:990-1004. http ://dx.doi.org /10.1016 /j.cell .2009.06.047
46. Hamada, T., H. Ueda, T. Kawase, and I. Hara-Nishimura. 2014. Microtubules contribute to tubule elongation and anchoring of endoplasmic reticulum, resulting in high network complexity in Arabidopsis. Plant Physiol. 166:1869-1876. http ://dx.doi.org /10.1104 /pp.114.252320
47. Hanna, M.G. IV, I. Mela, L. Wang, R.M. Henderson, E.R. Chapman, J.M. Edwardson, and A. Audhya. 2016. Sar1 GTPase activity is regulated by membrane curvature. J. Biol. Chem. 291:1014-1027. http ://dx.doi.org /10.1074 /jbc.M115.672287
48. Hansen, C.G., N.A. Bright, G. Howard, and B.J. Nichols. 2009. SDPR induces membrane curvature and functions in the formation of caveolae. Nat. Cell Biol. 11:807-814. http ://dx.doi.org /10.1038 /ncb1887
49. Hansen, C.G., G. Howard, and B.J. Nichols. 2011. Pacsin 2 is recruited to caveolae and functions in caveolar biogenesis. J. Cell Sci. 124:2777-2785. http ://dx.doi.org /10.1242 /jcs.084319
50. Hanson, P.I., R. Roth, Y. Lin, and J.E. Heuser. 2008. Plasma membrane deformation by circular arrays of ESC RT-III protein filaments. J. Cell Biol. 180:389-402. http ://dx.doi.org /10.1083 /jcb.200707031
51. Hariri, H., N. Bhattacharya, K. Johnson, A.J. Noble, and S.M. Stagg. 2014. Insights into the mechanisms of membrane curvature and vesicle scission by the small GTPase Sar1 in the early secretory pathway. J. Mol. Biol. 426:3811-3826. http ://dx.doi.org /10.1016 /j.jmb.2014.08.023
52. Harner, M., C. Körner, D. Walther, D. Mokranjac, J. Kaesmacher, U. Welsch, J. Griffith, M. Mann, F. Reggiori, and W. Neupert. 2011. The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J. 30:4356-4370. http ://dx.doi.org /10.1038 /emboj.2011.379
53. Helfrich, W. 1973. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C. 28:693-703.
54. Helfrich, P., and E. Jakobsson. 1990. Calculation of deformation energies and conformations in lipid membranes containing gramicidin channels. Biophys. J. 57:1075-1084. http ://dx.doi.org /10.1016 /S0006 -3495(90)82625 -4
55. Henne, W.M., H.M. Kent, M.G. Ford, B.G. Hegde, O. Daumke, P.J. Butler, R. Mittal, R. Langen, P.R. Evans, and H.T. McMahon. 2007. Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure. 15:839-852. http ://dx.doi.org /10.1016 /j.str.2007.05.002
56. Henne, W.M., E. Boucrot, M. Meinecke, E. Evergren, Y. Vallis, R. Mittal, and H.T. McMahon. 2010. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science. 328:1281-1284. http ://dx.doi.org /10.1126 /science .1188462
57. Henne, W.M., N.J. Buchkovich, Y. Zhao, and S.D. Emr. 2012. The endosomal sorting complex ESC RT-II mediates the assembly and architecture of ESC RT-III helices. Cell. 151:356-371. http ://dx.doi.org /10.1016 /j.cell .2012.08.039
58. Hoelz, A., E.W. Debler, and G. Blobel. 2011. The structure of the nuclear pore complex. Annu. Rev. Biochem. 80:613-643. http ://dx.doi.org /10.1146 / annurev -biochem -060109 -151030
59. Hu, J., Y. Shibata, C. Voss, T. Shemesh, Z. Li, M. Coughlin, M.M. Kozlov, T.A. Rapoport, and W.A. Prinz. 2008. Membrane proteins of the endoplasmic reticulum induce high-curvature tubules. Science. 319:1247-1250. http ://dx.doi.org /10.1126 /science.1153634
60. Hu, J., Y. Shibata, P.P. Zhu, C. Voss, N. Rismanchi, W.A. Prinz, T.A. Rapoport, and C. Blackstone. 2009. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell. 138:549-561. http ://dx .doi.org /10.1016 /j.cell.2009.05.025
61. Hunt, S.D., A.K. Townley, C.M. Danson, P.J. Cullen, and D.J. Stephens. 2013. Microtubule motors mediate endosomal sorting by maintaining functional domain organization. J. Cell Sci. 126:2493-2501. http ://dx.doi .org /10.1242 /jcs.122317
62. Isas, J.M., M.R. Ambroso, P.B. Hegde, J. Langen, and R. Langen. 2015. Tubulation by amphiphysin requires concentration-dependent switching from wedging to scaffolding. Structure. 23:873-881. http ://dx.doi.org /10 .1016 /j.str.2015.02.014
63. Iwai, M., M. Yokono, and A. Nakano. 2014. Visualizing structural dynamics of thylakoid membranes. Sci. Rep. 4:3768. http ://dx.doi.org /10.1038 / srep03768
64. Jao, C.C., B.G. Hegde, J.L. Gallop, P.B. Hegde, H.T. McMahon, I.S. Haworth, and R. Langen. 2010. Roles of amphipathic helices and the bin/ amphiphysin/rvs (BAR) domain of endophilin in membrane curvature generation. J. Biol. Chem. 285:20164-20170. http ://dx.doi.org /10.1074 /jbc.M110.127811
65. Jiko, C., K.M. Davies, K. Shinzawa-Itoh, K. Tani, S. Maeda, D.J. Mills, T. Tsukihara, Y. Fujiyoshi, W. Kühlbrandt, and C. Gerle. 2015. Bovine F1Fo ATP synthase monomers bend the lipid bilayer in 2D membrane crystals. eLife. 4:e06119. http ://dx.doi.org /10.7554 /eLife.06119
66. Jouhet, J. 2013. Importance of the hexagonal lipid phase in biological membrane organization. Front. Plant Sci. 4:494. http ://dx.doi.org /10.3389 /fpls.2013 .00494
67. Kabachinski, G., and T.U. Schwartz. 2015. The nuclear pore complex--structure and function at a glance. J. Cell Sci. 128:423-429. http ://dx.doi.org /10 .1242 /jcs.083246
68. Knox, K., P. Wang, V. Kriechbaumer, J. Tilsner, L. Frigerio, I. Sparkes, C. Hawes, and K. Oparka. 2015. Putting the squeeze on plasmodesmata: A role for reticulons in primary plasmodesmata formation. Plant Physiol. 168:1563-1572. http ://dx.doi.org /10.1104 /pp.15.00668
69. Krauss, M., J.Y. Jia, A. Roux, R. Beck, F.T. Wieland, P. De Camilli, and V. Haucke. 2008. Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J. Biol. Chem. 283:27717-27723. http ://dx.doi.org /10.1074 /jbc .M804528200
70. Kriechbaumer, V., S.W. Botchway, S.E. Slade, K. Knox, L. Frigerio, K. Oparka, and C. Hawes. 2015. Reticulomics: protein-protein interaction studies with two plasmodesmata-localized reticulon family proteins identify binding partners enriched at plasmodesmata, endoplasmic reticulum, and the plasma membrane. Plant Physiol. 169:1933-1945.
71. Kühn, S., C. Erdmann, F. Kage, J. Block, L. Schwenkmezger, A. Steffen, K. Rottner, and M. Geyer. 2015. The structure of FMNL2-Cdc42 yields insights into the mechanism of lamellipodia and filopodia formation. Nat. Commun. 6:7088. http ://dx.doi.org /10.1038 /ncomms8088
72. Kusumi, A., K.G. Suzuki, R.S. Kasai, K. Ritchie, and T.K. Fujiwara. 2011. Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36:604-615. http ://dx.doi.org /10.1016 /j.tibs.2011 .08.001
73. Lee, M.C., L. Orci, S. Hamamoto, E. Futai, M. Ravazzola, and R. Schekman. 2005. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COP II vesicle. Cell. 122:605-617. http ://dx.doi.org /10 .1016 /j.cell.2005.07.025
74. Lewellyn, E.B., R.T. Pedersen, J. Hong, R. Lu, H.M. Morrison, and D.G. Drubin. 2015. An engineered minimal WASP-myosin fusion protein reveals essential functions for endocytosis. Dev. Cell. 35:281-294. http ://dx.doi .org /10.1016 /j.devcel.2015.10.007
75. Liebe, S., and D. Menzel. 1995. Actomyosin-based motility of endoplasmic reticulum and chloroplasts in Vallisneria mesophyll cells. Biol. Cell. 85:207-222. http ://dx.doi.org /10.1016 /0248 -4900(96)85282 -8
76. Liu, A.P., D.L. Richmond, L. Maibaum, S. Pronk, P.L. Geissler, and D.A. Fletcher. 2008. Membrane-induced bundling of actin filaments. Nat. Phys. 4:789-793. http ://dx.doi.org /10.1038 /nphys1071
77. Llobet, A., J.L. Gallop, J.J. Burden, G. Camdere, P. Chandra, Y. Vallis, C.R. Hopkins, L. Lagnado, and H.T. McMahon. 2011. Endophilin drives the fast mode of vesicle retrieval in a ribbon synapse. J. Neurosci. 31:8512-8519. http ://dx.doi.org /10.1523 /JNE URO SCI.6223 -09.2011
78. Lundmark, R., G.J. Doherty, M.T. Howes, K. Cortese, Y. Vallis, R.G. Parton, and H.T. McMahon. 2008. The GTPase-activating protein GRAF1 regulates the CLIC/GEEC endocytic pathway. Curr. Biol. 18:1802-1808. http ://dx .doi.org /10.1016 /j.cub.2008.10.044
79. Manneville, J.B., J.F. Casella, E. Ambroggio, P. Gounon, J. Bertherat, P. Bassereau, J. Cartaud, B. Antonny, and B. Goud. 2008. COPI coat assembly occurs on liquid-disordered domains and the associated membrane deformations are limited by membrane tension. Proc. Natl. Acad. Sci. USA. 105:16946-16951. http ://dx.doi.org /10.1073 /pnas .0807102105
80. Masuda, M., S. Takeda, M. Sone, T. Ohki, H. Mori, Y. Kamioka, and N. Mochizuki. 2006. Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25:2889-2897. http ://dx.doi.org /10.1038 /sj.emboj.7601176
81. Matsuo, H., J. Chevallier, N. Mayran, I. Le Blanc, C. Ferguson, J. Fauré, N.S. Blanc, S. Matile, J. Dubochet, R. Sadoul, et al. 2004. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science. 303:531-534. http ://dx.doi.org /10.1126 /science .1092425
82. Mattila, P.K., and P. Lappalainen. 2008. Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9:446-454. http ://dx.doi.org /10.1038 /nrm2406
83. Mattila, P.K., A. Pykäläinen, J. Saarikangas, V.O. Paavilainen, H. Vihinen, E. Jokitalo, and P. Lappalainen. 2007. Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 176:953-964. http ://dx.doi.org /10.1083 /jcb .200609176
84. Maule, A., C. Faulkner, and Y. Benitez-Alfonso. 2012. Plasmodesmata "in Communicado". Front. Plant Sci. 3:30. http ://dx.doi.org /10.3389 /fpls .2012.00030
85. McBride, H.M., M. Neuspiel, and S. Wasiak. 2006. Mitochondria: more than just a powerhouse. Curr. Biol. 16:R551-R560. http ://dx.doi.org /10.1016 /j.cub.2006.06.054
86. McCullough, J., R.D. Fisher, F.G. Whitby, W.I. Sundquist, and C.P. Hill. 2008. ALIX-CHMP4 interactions in the human ESC RT pathway. Proc. Natl. Acad. Sci. USA. 105:7687-7691. http ://dx.doi.org /10.1073 /pnas .0801567105
87. McCullough, J., A.K. Clippinger, N. Talledge, M.L. Skowyra, M.G. Saunders, T.V. Naismith, L.A. Colf, P. Afonine, C. Arthur, W.I. Sundquist, et al. 2015. Structure and membrane remodeling activity of ESC RT-III helical polymers. Science. 350:1548-1551. http ://dx.doi.org /10.1126 /science.aad8305
88. McMahon, H.T., and E. Boucrot. 2015. Membrane curvature at a glance. J. Cell Sci. 128:1065-1070. http ://dx.doi.org /10.1242 /jcs.114454
89. McMahon, H.T., and J.L. Gallop. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature. 438:590-596. http ://dx.doi .org /10.1038 /nature04396
90. Mészáros, N., J. Cibulka, M.J. Mendiburo, A. Romanauska, M. Schneider, and A. Köhler. 2015. Nuclear pore basket proteins are tethered to the nuclear envelope and can regulate membrane curvature. Dev. Cell. 33:285-298. http ://dx.doi.org /10.1016 /j.devcel.2015.02.017
91. Miller, S.E., S. Mathiasen, N.A. Bright, F. Pierre, B.T. Kelly, N. Kladt, A. Schauss, C.J. Merrifield, D. Stamou, S. Höning, and D.J. Owen. 2015. CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev. Cell. 33:163-175. http ://dx.doi.org /10.1016 /j.devcel.2015.03.002
92. Monier, S., R.G. Parton, F. Vogel, J. Behlke, A. Henske, and T.V. Kurzchalia. 1995. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol. Biol. Cell. 6:911-927. http ://dx.doi.org /10.1091 /mbc.6.7.911
93. Morén, B., C. Shah, M.T. Howes, N.L. Schieber, H.T. McMahon, R.G. Parton, O. Daumke, and R. Lundmark. 2012. EHD2 regulates caveolar dynamics via ATP-driven targeting and oligomerization. Mol. Biol. Cell. 23:1316-1329. http ://dx.doi.org /10.1091 /mbc.E11 -09 -0787
94. Morlot, S., V. Galli, M. Klein, N. Chiaruttini, J. Manzi, F. Humbert, L. Dinis, M. Lenz, G. Cappello, and A. Roux. 2012. Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction. Cell. 151:619-629. http ://dx.doi.org /10.1016 /j.cell.2012.09.017
95. Morrow, I.C., and R.G. Parton. 2005. Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic. 6:725-740. http ://dx.doi .org /10.1111 /j.1600 -0854.2005.00318.x
96. Mullineaux, C.W. 2005. Function and evolution of grana. Trends Plant Sci. 10:521-525. http ://dx.doi.org /10.1016 /j.tplants.2005.09.001
97. Mustárdy, L., and G. Garab. 2003. Granum revisited. A three-dimensional model--where things fall into place. Trends Plant Sci. 8:117-122. http ://dx.doi.org /10.1016 /S1360 -1385(03)00015 -3
98. Peter, B.J., H.M. Kent, I.G. Mills, Y. Vallis, P.J. Butler, P.R. Evans, and H.T. McMahon. 2004. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science. 303:495-499. http ://dx.doi.org /10.1126 /science.1092586
99. Pfanner, N., M. van der Laan, P. Amati, R.A. Capaldi, A.A. Caudy, A. Chacinska, M. Darshi, M. Deckers, S. Hoppins, T. Icho, et al. 2014. Uniform nomenclature for the mitochondrial contact site and cristae organizing system. J. Cell Biol. 204:1083-1086. http ://dx.doi.org /10.1083 /jcb .201401006
100. Prévost, C., H. Zhao, J. Manzi, E. Lemichez, P. Lappalainen, A. Callan-Jones, and P. Bassereau. 2015. IRSp53 senses negative membrane curvature and phase separates along membrane tubules. Nat. Commun. 6:8529. http ://dx .doi.org /10.1038 /ncomms9529
101. Prinz, W.A., L. Grzyb, M. Veenhuis, J.A. Kahana, P.A. Silver, and T.A. Rapoport. 2000. Mutants affecting the structure of the cortical endoplasmic reticulum in Saccharomyces cerevisiae. J. Cell Biol. 150:461-474. http ://dx.doi.org /10.1083 /jcb.150.3.461
102. Puthenveedu, M.A., B. Lauffer, P. Temkin, R. Vistein, P. Carlton, K. Thorn, J. Taunton, O.D. Weiner, R.G. Parton, and M. von Zastrow. 2010. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell. 143:761-773. http ://dx.doi.org /10.1016 /j.cell.2010.10.003
103. Quader, H., A. Hofmann, and E. Schnepf. 1989. Reorganization of the endoplasmic reticulum in epidermal cells of onion bulb scales after cold stress: Involvement of cytoskeletal elements. Planta. 177:273-280. http ://dx.doi.org /10.1007 /BF00392816
104. Renard, H.F., M. Simunovic, J. Lemière, E. Boucrot, M.D. Garcia-Castillo, S. Arumugam, V. Chambon, C. Lamaze, C. Wunder, A.K. Kenworthy, et al. 2015. Endophilin-A2 functions in membrane scission in clathrinindependent endocytosis. Nature. 517:493-496. http ://dx.doi.org /10 .1038 /nature14064
105. Römer, W., L. Berland, V. Chambon, K. Gaus, B. Windschiegl, D. Tenza, M.R. Aly, V. Fraisier, J.C. Florent, D. Perrais, et al. 2007. Shiga toxin induces tubular membrane invaginations for its uptake into cells. Nature. 450:670-675. http ://dx.doi.org /10.1038 /nature05996
106. Rounds, C.M., and M. Bezanilla. 2013. Growth mechanisms in tip-growing plant cells. Annu. Rev. Plant Biol. 64:243-265. http ://dx.doi.org /10.1146 /annurev -arplant -050312 -120150
107. Roux, A., G. Cappello, J. Cartaud, J. Prost, B. Goud, and P. Bassereau. 2002. A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc. Natl. Acad. Sci. USA. 99:5394-5399. http ://dx.doi .org /10.1073 /pnas.082107299
108. Saarikangas, J., J. Hakanen, P.K. Mattila, M. Grumet, M. Salminen, and P. Lappalainen. 2008. ABBA regulates plasma-membrane and actin dynamics to promote radial glia extension. J. Cell Sci. 121:1444-1454. http ://dx.doi.org /10.1242 /jcs.027466
109. Saarikangas, J., H. Zhao, A. Pykäläinen, P. Laurinmäki, P.K. Mattila, P.K. Kinnunen, S.J. Butcher, and P. Lappalainen. 2009. Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr. Biol. 19:95-107. http ://dx.doi.org /10.1016 /j.cub.2008.12.029
110. Saarikangas, J., N. Kourdougli, Y. Senju, G. Chazal, M. Segerstråle, R. Minkeviciene, J. Kuurne, P.K. Mattila, L. Garrett, S.M. Hölter, et al. 2015. MIM-induced membrane bending promotes dendritic spine initiation. Dev. Cell. 33:644-659. http ://dx.doi.org /10.1016 /j.devcel.2015.04.014
111. Schmid, S.L., and M. Mettlen. 2013. Cell biology: Lipid switches and traffic control. Nature. 499:161-162. http ://dx.doi.org /10.1038 /nature12408
112. Senju, Y., Y. Itoh, K. Takano, S. Hamada, and S. Suetsugu. 2011. Essential role of PAC SIN2/syndapin-II in caveolae membrane sculpting. J. Cell Sci. 124:2032-2040. http ://dx.doi.org /10.1242 /jcs.086264
113. Shibata, Y., C. Voss, J.M. Rist, J. Hu, T.A. Rapoport, W.A. Prinz, and G.K. Voeltz. 2008. The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 283:18892-18904. http ://dx.doi.org /10.1074 /jbc.M800986200
114. Simpson, C., C. Thomas, K. Findlay, E. Bayer, and A.J. Maule. 2009. An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. Plant Cell. 21:581-594. http ://dx.doi.org /10.1105 /tpc.108.060145
115. Singer, S.J. 1972. A fluid lipid-globular protein mosaic model of membrane structure. Ann. N.Y. Acad. Sci. 195:16-23. http ://dx.doi.org /10.1111 /j .1749 -6632.1972.tb54780.x
116. Sparkes, I.A., L. Frigerio, N. Tolley, and C. Hawes. 2009. The plant endoplasmic reticulum: a cell-wide web. Biochem. J. 423:145-155. http ://dx.doi.org /10.1042 /BJ20091113
117. Stachowiak, J.C., E.M. Schmid, C.J. Ryan, H.S. Ann, D.Y. Sasaki, M.B. Sherman, P.L. Geissler, D.A. Fletcher, and C.C. Hayden. 2012. Membrane bending by protein-protein crowding. Nat. Cell Biol. 14:944-949. http ://dx.doi .org /10.1038 /ncb2561
118. Stachowiak, J.C., F.M. Brodsky, and E.A. Miller. 2013. A cost-benefit analysis of the physical mechanisms of membrane curvature. Nat. Cell Biol. 15:1019-1027. http ://dx.doi.org /10.1038 /ncb2832
119. Tilsner, J., K. Amari, and L. Torrance. 2011. Plasmodesmata viewed as specialised membrane adhesion sites. Protoplasma. 248:39-60. http ://dx .doi.org /10.1007 /s00709 -010 -0217 -6
120. van Weering, J.R., and P.J. Cullen. 2014. Membrane-associated cargo recycling by tubule-based endosomal sorting. Semin. Cell Dev. Biol. 31:40-47. http ://dx.doi.org /10.1016 /j.semcdb.2014.03.015
121. van Weering, J.R., R.B. Sessions, C.J. Traer, D.P. Kloer, V.K. Bhatia, D. Stamou, S.R. Carlsson, J.H. Hurley, and P.J. Cullen. 2012. Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J. 31:4466-4480. http ://dx.doi.org /10.1038 /emboj.2012.283
122. Voeltz, G.K., W.A. Prinz, Y. Shibata, J.M. Rist, and T.A. Rapoport. 2006. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell. 124:573-586. http ://dx.doi.org /10.1016 /j.cell.2005.11.047
123. Vollmer, B., A. Schooley, R. Sachdev, N. Eisenhardt, A.M. Schneider, C. Sieverding, J. Madlung, U. Gerken, B. Macek, and W. Antonin. 2012. Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J. 31:4072-4084. http ://dx.doi .org /10.1038 /emboj.2012.256
124. Vollmer, B., M. Lorenz, D. Moreno-Andrés, M. Bodenhöfer, P. De Magistris, S.A. Astrinidis, A. Schooley, M. Flötenmeyer, S. Leptihn, and W. Antonin. 2015. Nup153 recruits the Nup107-160 complex to the inner nuclear membrane for interphasic nuclear pore complex assembly. Dev. Cell. 33:717-728. http ://dx.doi.org /10.1016 /j.devcel.2015.04.027
125. Waterman-Storer, C.M., and E.D. Salmon. 1998. Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr. Biol. 8:798-807. http ://dx.doi.org /10 .1016 /S0960 -9822(98)70321 -5
126. Wollert, T., C. Wunder, J. Lippincott-Schwartz, and J.H. Hurley. 2009. Membrane scission by the ESC RT-III complex. Nature. 458:172-177. http ://dx.doi .org /10.1038 /nature07836